1. HPV Vaccine Initiation in an Area with Elevated Cervical Cancer Rates
A Survey of Parents of Adolescent Girls in North Carolina
Sami Gottlieb, MD, MSPH
Centers for Disease Control and Prevention
March 31, 2009

2. HPV Vaccine in Communities with Elevated Rates of Cervical Cancer
HPV vaccine holds great promise for reducing burden of cervical cancer in the U.S.
Recommended routine use in year-old girls
Especially important in communities with highest cervical cancer rates
Large racial disparities in cervical cancer
Often in underserved areas
Little is known about HPV vaccine uptake in these communities
Adolescents with greatest need may be least likely to receive it
HPV vaccine holds great promise for reducing the burden of cervical cancer and other HPV-related disease in the U.S. and is recommended for routine use in 11 and 12 year-old girls. HPV vaccine will be especially important in communities with the highest cervical cancer rates. There are large racial disparities in cervical cancer rates with black and Hispanic women disproportionately affected, and the highest rates often occur in medically underserved areas. Little is known about HPV vaccine uptake in these communities, and adolescents with the greatest need for HPV vaccine may be least likely to receive it.

3. Objective
To assess HPV vaccine uptake and potential barriers to vaccination in an area with elevated cervical cancer rates
Our objective was to assess HPV vaccine uptake and potential barriers to vaccination in an area with elevated cervical cancer rates.

4. Study Population
Survey of parents/guardians of year-old girls in 5 North Carolina counties
County inclusion criteria
Cervical cancer incidence >10 cases/100,000
Cervical cancer mortality >4 deaths/100,000
≥ 20% African American residents
Study counties
Other eligible counties
We conducted a survey of parents and guardians of year-old girls in 5 North Carolina counties. The study counties are shown in pink on this map. County inclusion criteria were cervical cancer incidence rates greater than 10 cases per 100,000 women and cervical cancer mortality rates greater than 4 deaths per 100,000, both of which are substantially higher than the national average. Eligible counties also had at least 20% African American residents. The 5 study counties were randomly selected from a group of eligible counties that clustered in the same, mostly rural region of Southeastern North Carolina.

5. Survey Methods
Summer 2007: telephone interviews with a stratified random sample of county households
Oversampled in African American, rural areas
Questions on HPV vaccine uptake, main reasons for not vaccinating, and intentions to vaccinate
Has your daughter had any shots of the HPV vaccine?
How likely are you to get your daughter the HPV vaccine in the next year?
Estimates weighted to incorporate study design and sampling methods
During the summer of 2007, which was a little over a year after HPV vaccine was licensed and about 6 months after publicly funded vaccine became available in North Carolina through the VFC program, we conducted telephone interviews with a stratified random probability sample of county households. We selected parents with a year-old daughter and oversampled in predominantly African American and rural areas. Interviews contained questions on HPV vaccine uptake, main reasons for not vaccinating, and intentions to vaccinate daughters. After brief information about what HPV vaccine is, parents were asked: Has your daughter had any shots of the HPV vaccine? After some brief additional information about recommendations for its use, parents were asked: How likely are you to get your daughter the HPV vaccine in the next year? All estimates were weighted to incorporate the study design and sampling methods.

6. Results: Study Population
889 parents interviewed (73% of 1,220 eligible)
Selected characteristics, parent
Mean age, years 41
Black/African American
38%
Hispanic 5%
Selected characteristics, daughter 14
Saw provider in last year
92%
Had preventive care visit in last year
83%
Provider recommended HPV vaccine
21%
Overall, 889 parents were interviewed, 73% of those eligible. This sample represented a population of parents with a mean age of 41 years. 38% reported their race/ethnicity as black or African American and 5% as Hispanic. The mean age of the daughters was 14 years. Despite being considered “underserved” with respect to cervical cancer rates, 92% of parents reported their daughters had seen a health care provider in the past year and 83% stated they had had a preventive care visit such as a physical or check-up in the last year.
According to the parents’ reports, a health care provider had recommended HPV vaccine for 21% of the daughters.

7. Percentage of Daughters that Had Received ≥1 Dose of HPV Vaccine
Characteristic N
% vaccinated
Odds ratio
(95% CI)
Overall
886
10.3
Age group, years
10-12
249
6.4
ref
13-15
290
7.5
1.2 ( )
16-18
339
17.5
3.1 ( )
Race/ethnicity
White
622
Black
205
12.5
1.2 ( )
Hispanic 28
1.0
0.1 ( )
This slide shows the percentage of daughters that had received at least one dose of HPV vaccine, out of 886 who had this information. CLICK
Overall, 10.3% of the parents reported that their daughters had received at least one dose. CLICK
Looking at this by the daughters’ age group, only 6.4% of the year-old daughters had received HPV vaccine, whereas 17.5% of year-old daughters had received it, a significant 3-fold difference. CLICK
Among whites, the percentage of vaccinated daughters was 10.3%. It was slightly higher among blacks, 12.5%, but these figures were not significantly different. Although the numbers of parents of Hispanic ethnicity were relatively small, very few appeared to have vaccinated daughters, a significantly lower percentage than either non-Hispanic whites or blacks.

8. Percentage of Daughters that Had Received ≥1 Dose of HPV Vaccine
Characteristic N
% vaccinated
Odds ratio
(95% CI)
Overall
886
10.3
Age group, years
10-12
249
6.4
ref
13-15
290
7.5
1.2 ( )
16-18
339
17.5
3.1 ( )
Race/ethnicity
White
622
Black
205
12.5
1.2 ( )
Hispanic 28
1.0
0.1 ( )
Overall, 10.3% of the parents reported that their daughters had received at least one dose. CLICK

9. Percentage of Daughters that Had Received ≥1 Dose of HPV Vaccine
Characteristic N
% vaccinated
Odds ratio
(95% CI)
Overall
886
10.3
Age group, years
10-12
249
6.4
ref
13-15
290
7.5
1.2 ( )
16-18
339
17.5
3.1 ( )
Race/ethnicity
White
622
Black
205
12.5
1.2 ( )
Hispanic 28
1.0
0.1 ( )
Looking at this by the daughters’ age group, only 6.4% of the year-old daughters had received HPV vaccine, whereas 17.5% of year-old daughters had received it, a significant 3-fold difference in vaccine initiation. CLICK

10. Percentage of Daughters that Had Received ≥1 Dose of HPV Vaccine
Characteristic N
% vaccinated
Odds ratio
(95% CI)
Overall
886
10.3
Age group, years
10-12
249
6.4
ref
13-15
290
7.5
1.2 ( )
16-18
339
17.5
3.1 ( )
Race/ethnicity
White
622
Black
205
12.5
1.2 ( )
Hispanic 28
1.0
0.1 ( )
Among whites, the percentage of vaccinated daughters was 10.3%. It was slightly higher among blacks, 12.5%, though these figures were not significantly different. Although the numbers of parents of Hispanic ethnicity were relatively small, very few appeared to have vaccinated daughters, significantly lower than either non-Hispanic whites or blacks.

11. Percentage of Daughters that Had Received ≥1 Dose of HPV Vaccine
Characteristic N
% vaccinated
Odds ratio
(95% CI)
Health insurance status
Private
733
9.1
ref
Public only
108
16.1
1.9 ( )
None 42
4.3
0.5 ( )
Health care provider
recommended vaccine No
684
4.2
Yes
193
34.0
11.7 ( )
This slide shows HPV vaccine uptake by daughters’ health insurance status and whether a health care provider had recommended HPV vaccine. CLICK
Those with public insurance only, that is, Medicaid or the state Children’s Health Insurance Program, had vaccine initiation of 16.1%, versus 9.1% among those with private insurance, though this difference was not significant. CLICK
Among those who had been recommended HPV vaccine by a health care provider, 34% had initiated it.

12. Percentage of Daughters that Had Received ≥1 Dose of HPV Vaccine
Characteristic N
% vaccinated
Odds ratio
(95% CI)
Health insurance status
Private
733
9.1
ref
Public only
108
16.1
1.9 ( )
None 42
4.3
0.5 ( )
Health care provider
recommended vaccine No
684
4.2
Yes
193
34.0
11.7 ( )
Those with public insurance only, that is, Medicaid or the state Children’s Health Insurance Program, had vaccine initiation of 16.1%, versus 9.1% among those with private insurance, though this difference was not significant. CLICK

13. Percentage of Daughters that Had Received ≥1 Dose of HPV Vaccine
Characteristic N
% vaccinated
Odds ratio
(95% CI)
Health insurance status
Private
733
9.1
ref
Public only
108
16.1
1.9 ( )
None 42
4.3
0.5 ( )
Health care provider
recommended vaccine No
684
4.2
Yes
193
34.0
11.7 ( )
Among those who had been recommended HPV vaccine by a health care provider, 34% had initiated vaccination.

14. Associations with HPV Vaccine Initiation in Multivariate Model
Only two factors independently associated with HPV vaccine initiation in multivariate model
Age group of daughter
16-18 vs year-olds: OR 3.1, 95% CI
Provider’s recommendation
Strongly associated: OR 12.6, 95% CI
Only 2 factors were independently associated with HPV vaccine initiation in a multivariate model. First, age group of the daughter year-old daughters were significantly more likely than year-olds to have initiated HPV vaccine. Second, a health care provider’s recommendation was strongly associated with HPV vaccine initiation.

15. Location and Costs of HPV Vaccination for Vaccinated Daughters (n=106)
Nothing
60%
≥$100 4%
<$100
35%
Out-of-pocket costs
Where received vaccine
Pediatrics
40%
Family
practice
23%
OB/gyn
19%
“Public
clinic”
10%
Military
facility 8%
40% of vaccinated daughters had received the vaccine from a pediatrician, 23% from a family practitioner, and 19% from an obstetrician-gynecologist. Another 10% of parents stated only that their daughter got HPV vaccine at a “public clinic” and 8% at a military facility. The majority, 60%, did not have any out of pocket costs when they got the first dose of vaccine; 35% paid less than $100, and only 4% paid close to the full $120 wholesale cost per dose.

16. Main Reasons Reported for Daughters Not Having Received Vaccine (n=780)
Few caregivers reported cost, insurance issues, or vaccine safety concerns as main reasons
Only 0.5% of caregivers cited concern about HPV vaccine making teenage girl more likely to have sex
Need more information about vaccine
22%
Never heard of vaccine
15%
Daughter is too young
16%
Daughter is not having sex yet
13%
Haven’t been to MD, gotten around to it yet
Now turning to the parents of unvaccinated daughters, this slide shows the main reasons parents reported for their daughters not having received HPV vaccine. We had this information for 780 parents. The most commonly cited reason was needing more information about the vaccine, reported by 22% of parents. An additional 15% reported that they had never heard of HPV vaccine or were not aware their daughter could get it.
Another commonly cited reason for not vaccinating was feeling the daughter was too young for HPV vaccine, reported by 16% of parents. This figure varied by the age group of the daughter. Only 3% of parents of year-olds cited this as a reason, but 27% of parents of year-olds did. An additional 13% of parents reported that they had not vaccinated because their daughter is not having sex yet.
Thirteen percent of parents reported that they just hadn’t been to the doctor or gotten around to it yet.
Few parents reported cost, insurance issues, or vaccine safety concerns as main reasons for not vaccinating. Only 0.5% of parents cited a concern that HPV vaccine may make a teenage girl more likely to have sex as a main reason for not vaccinating.

17. Intentions to Vaccinate: Parents with Unvaccinated Daughters (n=783)
62% reported that their daughters “probably” or “definitely” will get HPV vaccine in the next year
Only 10% reported that their daughters “definitely won’t” get it in the next year
No significant differences in intentions to vaccinate by age group of daughters
No significant differences by race/ethnicity
67% of blacks, 58% of whites, 66% of Hispanics/others intended to vaccinate
Among caregivers with unvaccinated daughters, 62% reported that their daughters “probably” or “definitely” will get HPV vaccine in the next year. Only 10% reported that their daughters “definitely won’t” get it in the next year. There were no significant differences in intentions to vaccinate by age group of daughters, despite notable differences in HPV vaccine initiation, and no significant differences by race/ethnicity. Sixty-seven percent of blacks and 58% of whites intended to vaccinate in the next year. Although few of their daughters had been vaccinated, 66% of Hispanics and others had intentions to vaccinate.

18. Limitations Generalizability Vaccination status reported by parent
Survey done soon after vaccine available
Still evolving, may not reflect current coverage
Follow-up survey 15 months after initial interviews: data will be presented at APHA meeting this fall
This study had several limitations that need to be considered. First, because we focused on an area with elevated cervical cancer rates in the Southeastern United States, findings from our study may not be generalizable to other populations. Second, vaccination status was reported by the parent and not confirmed by medical record review, so there may have been some recall and misclassification errors. Finally, as our survey was done relatively soon after vaccine became available, HPV vaccine initiation in this at-risk community is likely to still be evolving; the vaccine coverage I have discussed here may not reflect current coverage. We have recently completed a follow-up survey with these parents that was done approximately 15 months after the initial interviews to determine uptake of HPV vaccine over time and predictors of uptake. These data will be presented at the APHA meeting this fall, and should provide additional information on HPV vaccine coverage in this community at risk.

19. Summary
In at-risk population, only 10% of year-old daughters had initiated HPV vaccine
About 1 year after vaccine licensed and 6 months after publicly funded vaccine available
Older daughters more likely to have initiated
No racial disparities in vaccine initiation
Main reasons for not having vaccinated: needing more information, feeling daughter too young
Majority of parents with unvaccinated daughters intended for them to be vaccinated
To summarize, in this at-risk population with elevated cervical cancer rates, only 10% of parents reported their year-old daughters had initiated HPV vaccination, about 1 year after HPV vaccine was licensed and 6 months after publicly funded VFC vaccine became available in North Carolina. HPV vaccine initiation varied by age group of the daughter, with older daughters much more likely to have initiated vaccine than younger daughters. We observed no black-white racial disparities in HPV vaccine uptake. The main reasons reported for daughters not having been vaccinated revolved around two things: first, not being aware of the vaccine or needing more information about it, and second, feeling the daughter was too young or was not yet having sex. Despite the relatively low level of HPV vaccine initiation in this population, the majority of parents with unvaccinated daughters intended for them to be vaccinated in the next year.

20. Discussion and Implications
Vaccine coverage lower than the 25% coverage in population-based assessments in US and CA
2007 NIS—Teen and CHIS: collected data later
HPV vaccine initiation likely to be increasing over time, but differences are concerning
Differential uptake by age may reflect:
Desire to catch-up older teens
Perception that vaccine not yet needed in younger girls
Over one-quarter of parents of year-old girls had not vaccinated because felt daughters too young
Vaccine coverage with at least 1 dose of HPV vaccine in this at-risk population was substantially lower than the 25% vaccine coverage found in population-based assessments in the U.S. and California: the 2007 National Immunization Survey—Teen and the California Health Interview Survey. NIS—Teen collected data in the fourth quarter of 2007 and the California study had data collection into early HPV vaccine initiation is likely to be increasing over time, but the differences between our findings and those of the other studies are concerning. To have the greatest impact on disease prevention, vaccination rates will need to be optimized in communities with the highest cervical cancer rates.
Differential HPV vaccine uptake by age group may reflect a desire to provide catch-up vaccination for older teens as soon as possible, since these girls are closest to the risk of HPV infection and still within the age range covered by the VFC program. On the other hand, it may reflect a perception that the vaccine is not yet needed in younger teens. This latter perception appears to be playing a contributing role. Over one-quarter of parents of year-olds, the age group recommended for routine vaccination by the ACIP, reported that the main reason they had not vaccinated was because their daughters were too young. HPV vaccine is most efficacious in those who have never had HPV infection, and HPV is acquired rapidly following sexual debut. Parents typically fail to predict the timing of their daughters’ sexual initiation, so it is critical that parents and providers are educated about the need to follow ACIP guidelines to maximize the benefits of HPV vaccination.

21. Discussion and Implications
Lack of early racial disparities encouraging, could help close racial gaps in cervical cancer
Main barriers reported by parents can be overcome with information and education
Most parents intended to vaccinate
Additional efforts needed in communities with elevated cervical cancer rates
The lack of racial disparities in HPV vaccine initiation we observed was encouraging, given existing black-white racial disparities in cervical cancer. HPV vaccine could help close these racial gaps, and we need to work toward making that a reality.
Finally, the main barriers reported by parents in our population, such as needing more information about HPV vaccine and being concerned that their daughters are too young, can be overcome with information and education of parents and health care providers in these communities. Most parents with unvaccinated daughters, regardless of age, intended for them to be vaccinated in the next year. To have the greatest impact on cervical cancer and other HPV-related disease, additional efforts are needed in communities with elevated cervical cancer rates to ensure that intentions to vaccinate translate into HPV vaccination. Thank you.

22. NC Dept of HHS Immunization Branch UNC Survey Research Unit
Acknowledgments
UNC, Chapel Hill
Noel Brewer, PI
Karen Ziarnowski
Jennifer Smith
CDC
Lauri Markowitz
Maya Sternberg
Nicole Liddon
NC Dept of HHS Immunization Branch
Andrea Held
UNC Survey Research Unit
Robert Agans
William Kalsbeek
This study was carried out as part of the Carolina HPV Immunization Measurement and Evaluation project, or CHIME, led by Noel Brewer at UNC, Chapel Hill. I’d like to acknowledge him and our other collaborators listed here.
The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention.

24. Main Reasons for Not Receiving Vaccine among Those Recommended It by a Health Care Provider (n=115)
Daughter is too young
19%
Haven’t been to MD, gotten around to it yet
16%
Need more information about vaccine
15%
Vaccine not available yet 9%
Vaccine is too new 8%
Health insurance doesn’t cover vaccine